Anais da Academia Brasileira de Ciências (2019) 91(Suppl. 2): e20180643 (Annals of the Brazilian Academy of Sciences) Printed version ISSN 0001-3765 / Online version ISSN 1678-2690 http://dx.doi.org/10.1590/0001-3765201920180643 www.scielo.br/aabc | www.fb.com/aabcjournal

Osteohistology of the silesaurid Sacisaurus agudoensis from southern Brazil (Late ) and implications for growth in early

FÁBIO H. VEIGA1, JENNIFER BOTHA-BRINK2, ANA MARIA RIBEIRO1,3, JORGE FERIGOLO3 and MARINA B. SOARES1,4

1Programa de Pós-Graduação em Geociências, Instituto de Geociências, Universidade Federal do , Av. Bento Gonçalves, 9500, 91501-970 Porto Alegre, rS, Brazil 2Karoo Palaeontology Department, National Museum, Bloemfontein 9300, South Africa and Department of Zoology and Entomology, P.O. Box 266, University of the Free State, Bloemfontein 9300, South Africa 3Museu de Ciências Naturais, Fundação Zoobotânica do rio Grande do Sul, Av. Salvador França, 1427, 90690-000 Porto Alegre, rS, Brazil 4Departamento de Paleontologia e Estratigrafia, Instituto de Geociências, Universidade Federal do rio Grande do Sul, Av. Bento Gonçalves, 9500, 91501-970 Porto Alegre, rS, Brazil

Manuscript received on June 23, 2018; accepted for publication on September 16, 2018

How to cite: VEIGA Fh, BOthA-BrINK J, rIBEIrO AM, FErIGOLO J AND SOArES MB. 2019. Osteohistology of the silesaurid Sacisaurus agudoensis from southern Brazil () and implications for growth in early dinosaurs. An Acad Bras Cienc 91: e20180643. DOI 10.1590/0001-3765201920180643. Abstract: the non-dinosaurian dinosauriform silesaurids are the closest relatives of crown-group dinosaurs and are thus, important for understanding the origins of that group. here, we describe the limb bone histology of the Late triassic silesaurid Sacisaurus agudoensis from the Candelária Sequence of the Santa Maria Supersequence, Rio Grande do Sul state, Brazil. The sampled bones comprise eight femora and one fibula from different individuals. The microscopic analysis of all elements reveals uninterrupted fibrolamellar bone tissue indicating rapid growth. A transition to slower growing peripheral parallel-fibered bone tissue in some individuals indicates a decrease in growth rate, suggesting ontogenetic variation within the sample. the osteohistology of Sacisaurus agudoensis is similar to that of other silesaurids and supports previous hypotheses that rapid growth was attained early in the dinosauromorph lineage. however, silesaurids lack the complex vascular arrangements seen in saurischian dinosaurs. Instead, they exhibit predominantly longitudinally-oriented primary osteons with few or no anastomoses, similar to those of some small early ornithischian dinosaurs. this simpler vascular pattern is common to all silesaurids studied to date and indicates relatively slower growth rates compared to most Dinosauria. Key words: Archosauria, bone microstructure, dinosauriform, fibrolamellar bone, growth rates.

INTRODUCTION , as well as their extinct relatives. the early diversification of Archosauria occurred during Archosauria comprises extant crocodilians and the Middle triassic when they diverged into Correspondence to: Fábio hiratsuka Veiga two lineages: the crocodilian-line (Crurotarsi or E-mail: [email protected] Pseudosuchia) and the avian-line (Ornithosuchia, OrCid: http://orcid.org/0000-0003-3493-8542 * Contribution to the centenary of the Brazilian Academy of Ornithodira or Avemetatarsalia; see Gauthier Sciences. 1986, Sereno 1991, Benton 2004, Nesbitt et al.

EArth SCIENCES An Acad Bras Cienc (2019) 91(Suppl. 2) FÁBIO h. VEIGA et al. OStEOhIStOLOGY OF Sacisaurus agudoensis FrOM BrAZIL

2010). Ornithodira includes two clades, namely al. 2001), which is defined here by the presence Pterosauromorpha and (Langer of a woven-fibered bone matrix associated with and Benton 2006, Nesbitt 2011, Nesbitt et al. 2010). primary osteons, a tissue type that is indicative Within the latter, least inclusive clades, include the of relatively high rates of bone deposition and and the Dinosauria (Nesbitt 2011, growth rates (Francillon-Vieillot et al. 1990). the Langer et al. 2013). presence of growth marks [annuli and Lines of the (Langer et al. 2010, Nesbitt Arrested Growth (LAGs) indicating a temporary et al. 2010) were a diverse Middle to Late triassic decrease or cessation in growth, respectively, clade that are generally considered non-dinosaurian Francillon-Vieillot et al. 1990] varies considerably dinosauriforms (Ezcurra 2006, Irmis et al. 2007, in both groups, but most pseudosuchians tend to Brusatte et al. 2010, Nesbitt et al. 2010, Nesbitt exhibit cyclical growth from early ontogenetic 2011). however, its phylogenetic relationships to stages (ricqlès et al. 2003) whereas many derived Dinosauria is still debated in literature with the ornithodirans only express growth marks during suggestion that all or some silesaurid taxa fall the latest ontogenetic stages (e.g., neosauropod amongst the early members of the ornithischian dinosaurs, Klein and Sander 2008). lineage (Ferigolo and Langer 2007, Niedzwiedzki Studies on the osteohistology of dinosaurs et al. 2009, Langer and Ferigolo 2013, Cabreira et have increased dramatically in recent years (e.g., al. 2016). Grady et al. 2014, Vanderven et al. 2014, Cerda Given the discovery of new silesaurid et al. 2014, Bo et al. 2016, Mitchell et al. 2017, specimens (Kammerer et al. 2012, Peecook et Skutschas et al. 2017). however, given the relative al. 2013, Barrett et al. 2015) and the current scarcity of material, fewer studies encompassing debate regarding their phylogenetic relationships the taxa leading to crown-group dinosaurs have to Dinosauria, data on the life history of these been conducted. Previous descriptions on silesaurid can provide important new information on osteohistology include opolensis their biology and shed light on their similarities/ Dzik 2003 (Fostowicz-Frelik and Sulej 2010), differences to Dinosauria. the analysis of bone Asilisaurus kongwe Nesbitt et al. 2010 (Griffin microstructure or osteohistology of bones and Nesbitt 2016) and admixtus can provide such life history data by revealing romer 1972 (Marsà et al. 2017). these studies growth patterns and rates, ontogenetic stages and reveal similar bone tissues amongst the studied even biomechanical and hence lifestyle adaptations taxa, where uninterrupted fibrolamellar bone with of extinct animals (e.g., Enlow and Brown 1956, isolated primary osteons dominates. Griffin and 1957, 1958, ricqlès 1976, horner et al. 2000, Nesbitt (2016) suggested that the absence of LAGs Chinsamy-turan 2012, Padian and Lamm 2013, may be widespread amongst silesaurids and Marsà Legendre et al. 2016). et al. (2017) further proposed that these similarities Previous studies on the osteohistology of extant indicated that silesaurids shared similar life history and their extinct relatives have shown strategies. differences in the type of bone tissue deposition here, we present the first osteohistological between the two lineages of the group. Within the description of the Late triassic Brazilian silesaurid Pseudosuchia, lamellar bone, indicative of slow Sacisaurus agudoensis Ferigolo and Langer 2007. growth, is preponderant (ricqlès et al. 2003). In Given that few studies on the osteohistology of contrast, the bone tissues of the Ornithodira reveal silesaurids have been conducted to date, the data predominantly fibrolamellar bone (Padian et obtained from S. agudoensis provides an important

An Acad Bras Cienc (2019) 91(Suppl. 2) e20180643 2 | 17 FÁBIO h. VEIGA et al. OStEOhIStOLOGY OF Sacisaurus agudoensis FrOM BrAZIL contribution towards understanding the presumed been described in detail in previous studies (see similarities in their life histories and more broadly, Ferigolo and Langer 2007, Langer and Ferigolo the acquisition of early osteohistological 2013). characteristics and growth patterns. We analyzed nine limb bones, which comprise

MATERIALS AND METHODS eight right femora and one right incomplete fibula, all from different individuals. The complete femora INStItUtIONAL ABBrEVIAtIONS in the bone accumulation range from 85 mm to MCN PV – Museu de Ciências Naturais, Fundação 110 mm in length (Langer and Ferigolo 2013). We Zoobotânica do rio Grande do Sul, Brazil, sectioned one nearly complete femur (85 mm length, Paleovertebrates Collection. without the head) and seven incomplete femora,

MAtErIAL, LOCALItY AND hOrIZON where total length could not be measured (table I). however, comparing the width of the epiphyses the holotype and referred material of Sacisaurus with more complete femora found at the study agudoensis, was recovered from the Santa Maria locality showed that all the bones in our sample Supersequence, rio Grande do Sul State, Brazil. fall within this size range. the narrow size range the Late triassic Santa Maria Supersequence is composed of four third order sequences, from the and similar morphology suggest that all femora base to the top: Pinheiros-Chiniquá; Santa Cruz; represent individuals of a similar ontogenetic stage. Candelária and Mata (sensu horn et al. 2014), the to determine the ontogenetic stage of the elements first three being remarkable for their rich vertebrate in our sample, we compared the presence of fossil record. All specimens referred to S. agudoensis femoral scars in S. agudoensis with the landmarks were collected from a bone accumulation at a proposed by Griffin and Nesbitt (2016), who single outcrop located in the municipality of Agudo examined the development of bone scars across (Ferigolo and Langer 2007, Langer and Ferigolo a femoral ontogenetic series of the silesaurid 2013) assigned to the upper strata of the Candelária Asilisaurus kongue. All the known femora of S. sequence and the Assemblage Zone, agudoensis possess bone scars typical of skeletally in age (Soares et al. 2011, Langer et al. 2018). the lithology of this sedimentary package mature individuals of A. kongue, with the exception mostly consists of sandstones with isolated layers of of the trochanteric shelf, the linea intermuscularis mudstone and mud intraclasts, which is associated cranialis and the linea intermuscularis caudalis, with fluvial channel deposits (Zerfass et al. 2003, which are less developed in S. agudoensis. the horn et al. 2014). modest development of these scars suggests that Sacisaurus agudoensis is a small-bodied the femora of S. agudoensis do not belong to (less than 1 meter in body length), with fully grown individuals. the morphology alone is elongated distal hind limbs, an herbivorous/ an imprecise proxy in this case to determine the omnivorous diet and well-developed cursorial exact ontogenetic stage due to all the femora being abilities (see Langer and Ferigolo 2013). the bone accumulation of S. agudoensis shows a peculiar isolated and fragmented in the bone accumulation. preservation of over 30 nearly identical right femora One of the aims of this paleohistological analysis with only one left femur (see Langer and Ferigolo is to verify if these femora do belong to a single 2013). the morphology of the taxon has already ontogenetic stage.

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TABLE I Measurements, % vasc = percentage of vascularization, bone tissue type and preservation for the specimens examined in this study. Cross- Collection Proximal Distal sectional Element Number width width % vasc Bone tissue type Preservation diameter (MCN PV) (mm) (mm) (mm)

Fibula 10084 5.93 - 5.62 8.06 FLB Proximal half

Femur 10071 - 12.87 8.02 - FLB Distal quarter

Femur 10228 4.20 - 3.44 12.74 FLB Proximal half

Femur 10231 6.35 - 5.69 11.50 FLB Proximal quarter

Femur 10022 4.03 - 3.21 12.91 FLB/PFB Proximal three-fifths

Femur 10062 - 8.70 6.55 12.36 FLB/PFB No head

Femur 10070 - - 6.54 14.48 FLB/PFB Proximal quarter

Femur 10230 8.90 - 5.97 10.55 FLB/PFB Proximal quarter

Femur 10234 8.55 - 7.03 10.75 FLB/PFB Proximal half

PALEOhIStOLOGICAL PrOtOCOLS they were cut into smaller blocks perpendicular to the long axis of the bone using a cut-off diamond- transverse thin sections were made as close to the tipped saw within a Ken 9025 grinding machine. midshaft as possible as this region undergoes the One surface of each resin block was then affixed least secondary remodeling during growth and thus, to a frosted petrographic glass slide using the same provides the most complete growth record of the resin that was used for embedding and left to set for in long bones (Chinsamy 1990, Francillon- a further 24 hours. the sections were wet-ground Vieillot et al. 1990, Chinsamy and Dodson 1995, to approximately 60 µm thick and polished using horner et al. 1999). Photographs were taken prior to thin sectioning and measurements (cross-sectional a Prazis APL-S polishing machine with abrasive diameter, proximal/distal widths) are reported papers of increasing grit size (P80, P120, P320, in table I. the osteohistological thin sections P400, P600, P1200, P1500, P2000, P3000). were made at the Laboratório de Paleontologia IMAGE ANALYSIS de Vertebrados, Instituto de Geociências of the Universidade Federal do rio Grande do Sul, Porto the resulting thin sections were analyzed using a Alegre, Brazil, following standard methodological Leica DM 2500P microscope and photographed procedures outlined by Chinsamy and raath (1992), using an attached AxioCam Erc 5s camera. with adjustments. the bones were embedded in a the image analysis program NIh ImageJ 1.52e clear epoxy resin (Araldite© GY 279, catalyzed (Schneider et al. 2012) was used to quantify the with Aradur® hY 951) and left for 24 hours to set. degree of vascularization of the mid-cortex of

An Acad Bras Cienc (2019) 91(Suppl. 2) e20180643 4 | 17 FÁBIO h. VEIGA et al. OStEOhIStOLOGY OF Sacisaurus agudoensis FrOM BrAZIL each element allowing a quantitative comparison oriented canals (Figure 2a), with some short between the study specimens and other related radial and circumferential anastomoses (Figure groups in which similar data is available. Channel 2b). the vascularization of the mid-cortex varies area was measured in a field of view (FOV) taken from 10.6% to 14.5% (table I). Specimen MCN from the mid-cortex, divided by the total FOV area PV 10070 exhibits a more complex vascular and then converted into a percentage (Chinsamy arrangement, especially in the inner cortex, with 1993a). As already noted in the literature, radial and circumferential anastomoses reaching although the channels includes lymph, nerves a sub-reticular arrangement (Figure 2c-d). Small, and vascular canals that extend through the bone scattered secondary osteons were observed in most tissue (Mckenzie and Klein 2000), the calculation of the bones, but are mostly limited to the inner provides an estimation of the maximum amount cortex. however, the specimens, MCN PV 10230, of vascularization within a given section. We MCN PV 10231 and most notably MCN PV 10071, repeated the procedure for every third FOV at 10X exhibit large, abundant secondary osteons, but not magnification resulting in eight to ten FOV per to the extent of forming multi-generational dense slide, providing a good average of a given section. haversian bone. In MCN PV 10230 and PV 10231 terminology adopted follows that of Francillon- (Figure 3a and 3b, respectively) they appear locally, Vieillot et al. (1990), reid (1996), Chinsamy-turan on the medial side of the bone, whereas in MCN (2005, 2012) and Prondvai et al. (2014). PV 10071 (Figure 3c-d) they extend all around the medullary cavity and into the mid-cortex, RESULTS occupying approximately half of the compact

FEMOrA cortex. this region forms compacted coarse cancellous bone and is demarcated by a reversal the transverse thin sections of all femora reveal line (Figure 3d). the high degree of remodeling in a medullary cavity free of trabecular bone. Some these three bones reflects the region in which the elements (MCN PV 10022; PV 10062; PV 10228) thin sections were taken, which are the proximal are lateromedially compressed resulting in a (MCN PV 10230 and PV 10231) and distal (MCN flattened medullary cavity. This compression has PV 10071) metaphyses where remodeling tends to caused numerous cracks to extend through the be more prevalent. compact bone, but there are enough patches of well- Growth marks are absent from all the bones, preserved bone tissue to facilitate an assessment resulting in an uninterrupted fibrolamellar bone of the primary bone. A thick, irregular avascular complex. however, a peripheral area of slower endosteal layer of lamellar bone (Figure 1a-b) forming parallel-fibered bone can be seen in some surrounds the medullary cavity in all femora. of the femora (MCN PV 10022; PV 10062; PV the bone matrix exhibits regions of closely 10070; PV 10230; PV 10234). In these specimens, distributed haphazardly arranged globular the osteocyte lacunae near the bone periphery are osteocyte lacunae in a woven-fibered bone matrix flattened and more evenly distributed, running between primary osteons (Figure 1c-f). this parallel to one other (Figure 4a-h). the region also bone matrix indicates static osteogenesis and fast appears anisotropic in polarized light (Figure 4a- growth (Prondvai et al. 2014) and combined with f). In these elements, there is a slight decrease in the primary osteons acknoledges the presence the size and amount of the vascular canals towards of a fibrolamellar bone complex. the primary the peripheral region of the bone. the decreased osteons are predominantly isolated longitudinally- vascularization and transition to a parallel-fibered

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Figure 1 - Bone histology of femora of the Late triassic Sacisaurus agudoensis. a, b: thin-sections of MCN PV 10228 and PV 10022 respectively, showing layers of endosteal bone (arrow) in the perimedullary region; c, d, e and f: higher magnification of MCN PV 10228, PV 10022, PV 10231 and PV10234 respectively, showing primary osteons (black arrows) associated with the woven bone matrix and haphazardly osteocyte lacunae (white arrows). Abbreviations: mc, medullary cavity. Scale bars equal 100 µm.

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Figure 2 - Bone histology of femora of the Late triassic Sacisaurus agudoensis. a: thin-section of MCN PV 10228 showing isolated primary osteons through the cortex; b: thin-section of MCN 10062 showing primary osteons with short anastomoses (arrows); c, d: thin-sections of MCN PV 10070 showing the sub-reticular arrangement. Abbreviations: mc, medullary cavity. Scale bars equal 500 µm in a and c; 100 µm in b; 200 µm in d. bone matrix in the outer regions of the bone indicates (Figure 5a). the compact cortex also comprises a an overall decrease in the growth rate. however, the fibrolamellar bone complex with longitudinally- absence of an External Fundamental System (EFS, oriented primary osteons in a woven bone matrix sensu Cormack 1987) suggests that these bones (Figure 5c). the primary osteons are mostly isolated were not fully grown as an EFS generally indicates with short anastomoses and the bone tissues are the achievement of maximum size. less vascularized (8.1%) than the femora (average FIBULA = 12.2%). Vascularization remains constant throughout the cortex and there are no interruptions An incomplete fibula (MCN PV 10084, Figure in the bone tissue (Figure 5d). Scattered secondary 5a-d) was thin sectioned for this study. the most osteons are mostly limited to the inner cortex. As in striking feature of the bone is a broad and rugose “tibial flange” extending obliquely from its the femora an EFS is absent. the most conspicuous cranioproximal corner (see Langer and Ferigolo difference between the bone tissues of the fibula 2013: Figure 19f). and femora is the absence of an endosteal layer Similar to the femora, the medullary cavity surrounding the medullary cavity in the fibula of the fibula is completely free of trabecular bone (Figure 5a and 5b).

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Figure 3 - Bone histology of femora of the Late triassic Sacisaurus agudoensis. a, b: thin-sections of MCN PV 10230 and MCN PV 10231 respectively, showing compacted coarse cancellous bone and secondary osteons (arrows); c: thin section of MCN PV 10071 showing compacted coarse cancellous bone in the perimedullary region; d: higher magnification of MCN PV 10071 showing compacted coarse cancellous bone demarcated by a reversal line (white arrow) and secondary osteon (black arrow). Abbreviation: mc, medullary cavity. Scale bars equal 200 µm in a, b and d; 500 µm in c.

DISCUSSION that the circumferential endosteal lamellae indicates

ONtOGENEtIC StAGE OF thE StUDIED a temporary cessation in medullary expansion, after INDIVIDUALS which growth would have resumed. the presence of fibrolamellar bone, even at the sub-periosteal the analysis of the bone tissues of the study surface in some elements, indicates that these material reveals similar osteohistological features animals were still growing at the time of death. and thus suggests that the elements represent a Some femora (MCN PV 10022; PV 10062; PV similar ontogenetic stage. All elements, apart 10070; PV 10230; PV 10234) exhibit a transition from the fibula, exhibit a thick avascular endosteal from an inner woven bone matrix to an outer layer of lamellar bone surrounding the medullary cavity. this structure, as well as an EFS, has been parallel-fibered bone matrix. This transition from observed in the femora of mature individuals of fast to slower growing bone, as well the decrease in the silesaurid Silesaurus opolensis (Fostowicz- size and abundance of vascular canals towards the Frelik and Sulej 2010), indicating the cessation of bone periphery is evidence of a decrease in growth medullar expansion and thus, a mature ontogenetic rate, which indicates a departure from the juvenile age (Chinsamy-turan 2005). however, in the case stage into at least an early subadult stage for these of S. agudoensis, the absence of an EFS suggests individuals.

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Figure 4 - Bone histology of femora of the Late triassic Sacisaurus agudoensis. a: thin-section of MCN PV 10022 showing the transition from fibrolamellar bone in the inner cortex to parallel-fibered bone in the outer cortex; b: same region as a in polarized light highlighting the parallel-fibered bone; c: thin-section of MCN PV 10230 showing the transition from fibrolamellar bone to parallel-fibered bone; d: same region as c in polarized light highlighting the parallel-fibered bone; e: thin-section of MCN PV 10234 showing the transition from fibrolamellar bone to parallel-fibered bone;f : same region as e in polarized light highlighting the parallel-fibered bone;g : high magnification of MCN PV 10062 showing the transition from fibrolamellar bone to parallel-fibered bone;h : high magnification of MCN PV 10070 showing the transition from fibrolamellar bone to parallel-fibered bone. Abbreviations: flb, fibrolamellar bone; pfb, parallel-fibered bone. Scale bars equal 100 µm in a, b, c, d, e and f; 50 µm in g and h.

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Figure 5 - Bone histology of a fibula (MCN PV 10084) of the Late TriassicSacisaurus agudoensis. a: thin-section showing an open medullary cavity free of trabecular bone (note the absence of endosteal bone around the medullary cavity); b: high magnification showing primary osteons in the inner cortex (arrow); c: mid-cortical fibrolamellar bone with transversal osteocyte lacunae black( arrow) and primary osteons (white arrow); d: primary osteon (arrow) in the outer cortex (note how the vascularization is continuous and uniform towards the bone periphery). Abbreviations: mc, medullary cavity. Scale bars equal 400 µm in a; 200 µm in b; 100 µm in c and d.

The transverse thin section of the fibula MCN bone. the presence of this tissue type indicates PV 10084 lacks all features indicating an older relatively high rates of bone deposition and hence ontogenetic stage with only scattered secondary growth (Amprino 1947, Francillon-Vieillot et al. osteons appearing mainly in the inner cortex. there 1990, Margerie et al. 2002, Padian and Lamm 2013, is no decrease in vascularization and no change to Prondvai et al. 2014). the compact bone comprises slower forming parallel-fibered bone towards the isolated longitudinally-oriented primary osteons outer surface. Although vascularization is lower with some short anastomoses and a high density of than in the femora, the uniformity of the rapidly globular osteocyte lacunae. Fibrolamellar bone has forming fibrolamellar bone throughout the cortex been found in all other silesaurids studied to date supports a juvenile status for this individual. and the vascular pattern in S. agudoensis is similar to that observed in other taxa, such as Silesaurus GrOWth PAttErN AND COMPArISON WIth OthEr opolensis (Fostowicz-Frelik and Sulej 2010), Asilisaurus kongwe (Griffin and Nesbitt 2016) the bone tissues of Sacisaurus agudoensis are and Lewisuchus admixtus (Marsà et al. 2017). primarily composed of uninterrupted fibrolamellar However, it differs slightly from S. opolensis and

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L.admixtus in having more anastomoses connecting cortex being comprised of slowly forming lamellar- the longitudinal primary osteons. zonal bone (Mukherjee 2015, Veiga et al. 2015). Given the onset of peripheral parallel-fibered the tibia from an adult individual of the slightly bone in some individuals of S. agudoensis and more derived Early triassic archosauromorph absence of growth marks in all the bones studied, Prolacerta broomi Parrington 1935, exhibits a it is clear that it grew continuously (Padian and vascular pattern similar to that found in silesaurids Lamm 2013) to at least the subadult stage of its in which the longitudinally-oriented primary ontogeny. Growth marks have been observed osteons are mostly isolated with a few anastomoses within peripheral parallel-fibered bone in the (Botha-Brink and Smith 2011). however, the bone largest specimen of Silesaurus opolensis, however, tissues are notably less vascularized (e.g. 2.2% (Fostowicz-Frelik and Sulej 2010) and thus, it is compared to an average of 11% in S. agudoensis possible that S. agudoensis exhibited cyclical ) and combined with the prevalence of a mixture growth during later ontogenetic stages, but material of weakly developed fibrolamellar and parallel- from older individuals is required to test this. fibered bone, these features suggest lower growth the growth patterns of silesaurids differ rates in P. broomi (Botha-Brink and Smith 2011). from that seen in stem archosaurs, i.e., non- Fibrolamellar bone becomes more prevalent archosaurian archosauromorphs (Figure 6). For in the non-archosaurian archosauriforms. example, the osteohistology of the Late triassic Proterosuchus fergusi Broom 1903, a medium- Trilophosaurus buettneri Case 1928, described by sized proterosuchid (nearly 2 m in body length, Werning and Irmis (unpublished data), comprises Botha-Brink and Smith 2011), exhibits highly poorly vascularized lamellar bone with multiple vascularized (e.g. femoral vascularity 15%) LAGs throughout the cortex, indicating a slow radiating vascular canals within fibrolamellar growth rate. rhynchosauria osteohistology also bone during early ontogeny. Growth decreases indicates slow growth rates. For example, Werning dramatically during late ontogeny, however, with and Nesbitt (2015) described the osteohistology the onset of poorly vascularized lamellar-zonal bone of a femur and tibia from a mature individual of (Botha-Brink and Smith 2011). An unidentified the Middle triassic Stenaulorhynchus stockleyi long bone of the proterochampsid Chanaresuchus haughton 1932 from tanzania as moderate to bonapartei romer 1971 reveals similar bone poorly vascularized parallel-fibered bone tissue. tissues, but with a more sub-reticular vascular Similar bone tissues have also been found in the arrangement in the inner cortex (ricqlès et al. ribs of Hyperodapedon sanjuanensis Langer and 2008). Several elements from different individuals Schultz 2000 (previously Scaphonyx sanjuanensis of the large-bodied triassic erythrosuchids Sill 1970) from the Late triassic of Argentina Erythrosuchus africanus Broom 1905 (Gross 1934, (Ricqlès et al. 2008). Fast growing fibrolamellar ricqlès 1976, ricqlès et al. 2008, Botha-Brink bone has been observed in several elements and Smith 2011) and Garjainia madiba Gower et of some Late triassic rhynchosaurs, such as al. 2014 (Gower et al. 2014) exhibit a variety of Teyumbaita sulcognathus Montefeltro, Langer vascular arrangements including laminar, reticular and Schultz 2010 and Hyperodapedon sp. huxley and radial, within a fibrolamellar bone complex, 1859 from southern Brazil (Veiga et al. 2015), and indicating rapid growth rates, similar to those Hyperodapedon sp. from India (Mukherjee 2015). found in fast-growing dinosaurs. Although faster However, the fibrolamellar bone in these taxa is growing tissues become more prevalent among restricted to the innermost cortex, the rest of the non-archosaurian archosauriforms, it should be

An Acad Bras Cienc (2019) 91(Suppl. 2) e20180643 11 | 17 FÁBIO h. VEIGA et al. OStEOhIStOLOGY OF Sacisaurus agudoensis FrOM BrAZIL . * indicates the possible phylogenetic position the possible phylogenetic blue . * indicates axa cited in the text appear in . t . axa examined in this study appear in redin this study appear axa examined t (modified from Langer and Benton 2006, Nesbitt 2011, Otero et al. 2015, Ezcurra 2016) shows the microstructure of long bone along and b : FLB, fibrolamellar bone; LZB, lamellar-zonal bone; PFB, parallel-fibered bone. : FLB, fibrolamellar bone; LZB, lamellar-zonal of . Abbreviations Figure 6 - Cladogram a Figure by bone histology. Archosauromorpha as revealed

An Acad Bras Cienc (2019) 91(Suppl. 2) e20180643 12 | 17 FÁBIO h. VEIGA et al. OStEOhIStOLOGY OF Sacisaurus agudoensis FrOM BrAZIL noted that there are exceptions. For example, exhibits parallel-fibered bone (Butler et al. 2010) the Middle triassic Euparkeria capensis Broom and S. lawleri contains very little fibrolamellar 1913 exhibits predominantly low to moderately bone during early ontogeny and entirely lamellar- vascularized (3.3 to 5.4 %) parallel-fibered bone zonal bone during adulthood (Padian et al. 2004). (Botha-Brink and Smith 2011) and the Late Both taxa contain predominantly longitudinally- triassic Vancleavea campi Long and Murry 1995 oriented vascular canals with few anastomoses. contains poorly vascularized lamellar-zonal bone these ornithischians are relatively small, with F. tissue (Nesbitt et al. 2009). these taxa show that haagarorum only growing to a maximum length of there was some degree of experimentation amongst 75 cm and S. lawleri less than 1.5 m (Padian et al. the triassic non-archosaurian archosauriforms as 2004, Butler et al. 2010) and thus, body size may shown by the variety of bone tissue patterns in have played a role in their relatively slower growth this group. however, the increasing prevalence rates (Padian et al. 2004). For example, Padian et of highly vascularized fibrolamellar bone shows al. (2004) showed that the vascular arrangements that rapid growth rates evolved before the origin of of the bone tissues in small dinosaurs are simpler Ornithodira (ricqlès et al. 2008, Botha-Brink and and less vascularized compared to their larger Smith 2011, Gower et al. 2014) and is considered relatives (Singh et al. 1974, Case 1978). however, plesiomorphic for archosauriforms (ricqlès et al. the fabrosaurid L. diagnosticus, was also relatively 2003). small with an approximate body length of 2 m the simpler vascular pattern seen in (Knoll et al. 2010). It displays rapidly forming silesaurids differs from most early dinosaurs where fibrolamellar bone with longitudinally-oriented the vascular arrangements tend to exhibit more primary osteons during early ontogeny and a complex anastomosing. For example, plexiform laminar vascular arrangement during mid-ontogeny and laminar vascular patterns are typical of (Knoll et al. 2010), typical of other early saurischian early saurischian dinosaurs [e.g., dinosaurs. thus, factors other than body size likely ischigualastensis reig 1963, (Padian et al. 2001, played a role in shaping ornithischian growth rates 2004, ricqlès et al. 2003)], early sauropodomorphs and more research is required to better understand [e.g., Plateosaurus engelhardti Meyer 1837, the life histories of these taxa. Mussaurus patagonicus Bonaparte and Vince 1979, Although there are relatively few studies Massospondylus carinatus Owen 1854, (Klein and on the osteohistology of silesaurids and early Sander 2007, Cerda et al. 2014, Chinsamy, 1993b, dinosaurs, the data available to date suggest that respectively)] and the coelophysid neotheropod a simpler vascular arrangement of longitudinally- (Chinsamy 1990, ricqlès et al. 2003, Padian et al. oriented primary osteons is typical of silesaurids. 2004) Megapnosaurus rhodesiensis Ivie et al. 2001 In contrast, most early dinosaurs examined to (previously Syntarsus rhodesiensis raath 1969), date [apart from the contentious Nyasasaurus as well as the early ornithischian Lesothosaurus parringtoni (Nesbitt et al. 2013)] show a more diagnosticus Galton 1978 (specimen NMQr 3076, complex vascular arrangement early in their life Knoll et al. 2010). history. Given that more complex vascular patterns In contrast, the osteohistology of some early are associated with higher growth rates (Margerie et ornithischians such as the heterodontosaurid al. 2002, Padian and Lamm 2013), this implies that Fruitadens haagarorum Butler et al. 2010 and the silesaurids grew relatively more slowly than the thyreophoran Scutellosaurus lawleri Colbert 1981 earliest crown-group dinosaurs (apart from some exhibit slower forming bone tissues. F. haagarorum small ornithischians). Again, this may be related to

An Acad Bras Cienc (2019) 91(Suppl. 2) e20180643 13 | 17 FÁBIO h. VEIGA et al. OStEOhIStOLOGY OF Sacisaurus agudoensis FrOM BrAZIL body size because based on femoral length (sensu in other silesaurids. Our study supports previous Irmis 2011, turner and Nesbitt 2013, Piechowski studies in showing that high growth rates were et al. 2014, Barrett et al. 2015), all silesaurids already present prior the evolution of Ornithodira. studied to date were small-bodied species (body however, the simpler vascular pattern of length of approximately 1.5 m or less, Barrett et al. longitudinally-oriented primary osteons with few 2015), whereas early sauropodomorph dinosaurs anastomoses differs from the complex arrangements with more complex anastomoses were larger (Irmis generally found in crown-group dinosaurs. this 2011, turner and Nesbitt 2013). however, as suggests that silesaurids grew comparatively noted with L. diagnosticus some taxa do not show more slowly than most dinosaurs, which may be correlation between body size and vascularization. related to phylogeny or smaller body sizes. Further the coelophysid neotheropod M. rhodesiensis examination of more dinosauromorph taxa is also exhibits highly vascularized, complex required to confirm this hypothesis. arrangements despite having a similar body size to ACKNOWLEDGMENTS S. opolensis (Padian et al. 2001, Irmis 2011, turner and Nesbitt 2013). We thank Dr. C.S. Vega from the Universidade Additionally, Barrett et al. (2015) described the Federal do Paraná (UFPr) and the Laboratório de first larger-bodied silesaurid (NHMUK R16303) Pesquisa em Microscopia of UFPr for access to from the Lifua Member of the Manda Beds of imaging equipment. We also thank two anonymous tanzania, estimated to have had a femoral length of reviewers for their suggestions and comments. approximately 345 mm (body length estimated to be the Fundação de Amparo à Pesquisa do Estado approximately 3 m), which according to the authors, do rio Grande do Sul (FAPErGS) provided may represent a large individual of Asilisaurus financial support to FHV, MBS and JBB (Grant kongwe. the osteohistology of A. kongwe indicates number 0441-2551/14-7), the Coordenação de that the specimens were still growing at the time Aperfeiçoamento de Pessoal de Nível Superior of death and thus probably represent juveniles or (CAPES) provided financial support to FHV, the subadult individuals (Griffin and Nesbitt 2016). Conselho Nacional de Desenvolvimento Científico the material we sampled here also indicates e Tecnológico (CNPq) provided financial support that the bones came from juveniles and subadult to MBS (Grant number 312387/2016-4), to AMr individuals that were still growing. this suggests (Grant number 306951/2017-7) and the National that some silesaurids reached larger body sizes research Foundation (UID 98819 and 104688), than previously thought. Further osteohistological the Palaeontological Scientific trust (PASt), descriptions of such large specimens will clarify Johannesburg, South Africa, and DSt-NrF the correlation between body size and vascular Centre of Excellence in Palaeosciences (CoE-Pal) pattern among silesaurids. provided financial support to JBB.

CONCLUSIONS AUTHOR CONTRIBUTIONS the bone tissues of the non-dinosaurian Fábio hiratsuka Veiga, Jennifer Botha-Brink and dinosauriform silesaurid S. agudoensis exhibit Marina Bento Soares are responsible for the study rapidly forming fibrolamellar bone with conception, data analysis and to the writing of the longitudinally-oriented primary osteons and manuscript with input from the other authors. Fábio occasional anastomoses similar to that observed hiratsuka Veiga, Ana Maria ribeiro and Jorge

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